In vivo confocal microscopy of corneal nerves: Analysis and clinical correlation

Seminars in Ophthalmology

Volumn 25, Issue 5-6, 2010, Pages 171-177

  Cruzat, Andrea ^a   Pavan Langston, Deborah ^a   Hamrah, Pedram ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

confocal microscopy; cornea; esthesiometry; innervation; nerves; sensation

Indexed keywords

ARTICLE; CONFOCAL MICROSCOPY; CONTACT LENS; CORNEA NERVE; CORNEA SURGERY; CORNEA TRANSPLANTATION; DRY EYE; HUMAN; IMAGE ANALYSIS; IN VIVO CONFOCAL MICROSCOPY; IN VIVO STUDY; KERATITIS; KERATOCONUS; KERATOMILEUSIS; KERATOPATHY; LASER EPITHELIAL KERATOMILEUSIS; MEDLINE; NERVE FUNCTION; NERVE PLEXUS; OPTIC NERVE; PHOTOREFRACTIVE KERATECTOMY; PRIORITY JOURNAL;

CORNEA; CORNEAL DISEASES; HUMANS; MICROSCOPY, CONFOCAL; OPHTHALMIC NERVE;

EID: 78649372030     PISSN: 08820538     EISSN: 17445205     Source Type: Journal    
DOI: 10.3109/08820538.2010.518133     Document Type: Article

References (69)

1. Oliveira-Soto L, Efron N. Morphology of corneal nerves using confocal microscopy. Cornea 2001;20:374-384.
2. Guthoff RF, Wienss H, Hahnel C, Wree A. Epithelial inner-vation of human cornea: a three-dimensional study using confocal laser scanning fuorescence microscopy. Cornea 2005;24:608-613.
3. Beuerman RW, Schimmelpfennig B. Sensory dennervation of the rabbit cornea affects epithelial properties. Exp Neurol. 1980;69:196-201.
4. Stern ME, Beuerman RW, Fox RI, Gao J, Mircheff AK, Pfugfelder SC. The pathology of dry eye: the interaction between the ocular surface and lacrimal glands. Cornea. 1998;17:584-589.
5. Nishida T. Neurotrophic mediators and corneal wound healing. Ocul Surf 2005;3:194-202.
6. Müller LJ, Marfurt CF, Kruse F, Tervo TM. Corneal nerves: structure, contents and function. Exp Eye Res. 2003;76:521-542.
7. Müller LJ, Vrensen GF, Pels L, Cardozo BN, Willekens B. Architecture of human corneal nerves. Invest Ophthalmol Vis Sci. 1997;38:985-994.
8. Patel DV, McGhee CN. In vivo confocal microscopy of human corneal nerves in health, in ocular and systemic disease, and following corneal surgery: a review. Br J Ophthalmol. 2009;93:853-860.
9. Patel DV, McGhee CN. Contemporary in vivo confocal microscopy of the living human cornea using white light and laser scanning techniques: a major review. Clin Exp Ophthalmol. 2007;35:71-88.
10. Lemp MA, Dilly PN, Boyde A. Tandem-scanning (con-focal) microscopy of the full-thickness cornea. Cornea 1985;4:205-209.
11. Bochert R, Zhivov A, Kraak R, Stave J, Guthoff RF. Contribution to comprehension of image formation in con-focal microscopy of cornea with Rostock cornea module. Br J Ophthalmol. 2005;89:1351-1355.
12. Grupcheva CN, Wong T, Riley AF, McGhee CN. Assessing the sub-basal nerve plexus of the living healthy human cornea by in vivo confocal microscopy. Clin Exp Ophthalmol.2002;30:187-190.
13. Patel DV, McGhee CN. Mapping of the normal human cor-neal sub-Basal nerve plexus by in vivo laser scanning confocal microscopy. Invest Ophthalmol Vis Sci. 2005;46:4485-4488.
14. Patel DV, Tavakoli M, Craig JP, Efron N, McGhee CN. Corneal sensitivity and slit scanning in vivo confocal microscopy of the subbasal nerve plexus of the normal central and peripheral human cornea. Cornea 2009;28:735-740.
15. Millodot M. The infuence of age on the sensitivity of the cornea. Invest Ophthalmol Vis Sci. 1977;16:240-242.
16. Roszkowska AM, Colosi P, Ferreri FM, Galasso S. Age-related modifcations of corneal sensitivity. Ophthalmologica 2004;218:350-355.
17. Erie JC, McLaren JW, Hodge DO, Bourne WM. The effect of age on the corneal subbasal nerve plexus. Cornea 2005;24:705-709.
18. Niederer RL, Perumal D, Sherwin T, McGhee CN. Age-related differences in the normal human cornea: a laser scanning in vivo confocal microscopy study. Br J Ophthalmol. 2007;91:1165-1169.
19. Murphy PJ, Patel S, Marshall J. The effect of long-term, daily contact lens wear on corneal sensitivity. Cornea 2001;20:264-269
20. Patel SV, McLaren JW, Hodge DO, Bourne WM. Confocal microscopy in vivo in corneas of long-term contact lens wearers. Invest Ophthalmol Vis Sci. 2002;43:995-1003.
21. Oliveira-Soto L, Efron N. Morphology of corneal nerves in soft contact lens wear. A comparative study using confocal microscopy. Ophthalmic Physiol Optics 2003;23:165-174.
22. Millodot M. Effect of long-term wear of hard contact lenses on corneal sensitivity. Arch Ophthalmol. 1978;96:1225-1227. (Pubitemid 8371570)
23. Niederer R, McGhee C. Clinical in vivo confocal microscopy of the human cornea in health and disease. Prog Retin Eye Res. 2009; Nov 26. [Epub ahead of print] PMID: 19944182.
24. Edwards M, McGhee CN, Dean S. The genetics of keratoco-nus. Clin Exp Ophthalmol. 2001;29:345-351.
25. Patel DV, McGhee CN. Mapping the corneal sub-basal nerve plexus in keratoconus by in vivo laser scanning confocal microscopy. Invest Ophthalmol Vis Sci. 2006;47:1348-1351.
26. Patel DV, Ku JY, Johnson R, McGhee CN. Laser scanning in vivo confocal microscopy and quantitative aesthesiom-etry reveal decreased corneal innervation and sensation in keratoconus. Eye 2009;23:586-592.
27. Niederer RL, Perumal D, Sherwin T, McGhee CN. Laser scanning in vivo confocal microscopy reveals reduced inner-vation and reduction in cell density in all layers of the kerato-conic cornea. Invest Ophthalmol Vis Sci. 2008;49:2964-2970.
28. Simo Mannion L, Tromans C, O'Donnell C. An evaluation of corneal nerve morphology and function in moderate kera-toconus. Contact Lens Anterior Eye 2005; 28:185-192.
29. Mocan MC, Yilmaz PT, Irkec M, Orhan M. In vivo confocal microscopy for the evaluation of corneal microstructure in keratoconus. Curr Eye Res. 2008;33:933-939.
30. Hollingsworth JG, Efron N, Tullo AB. In vivo corneal con-focal microscopy in keratoconus. Ophthalmic Physiol Opt. 2005;25:254-260.
31. Brookes NH, Loh IP, Clover GM, Poole CA, Sherwin T. Involvement of corneal nerves in the progression of kera-toconus. Exp Eye Res. 2003;77: 515-524.
32. Xu K P, Yagi Y, Tsubota K. Decrease in corneal sensitivity and change in tear function in dry eye. Cornea. 1996;15:235-239.
33. Hosal BM, Ornek N, Zilelioglu G, Elhan AH. Morphology of corneal nerves and corneal sensation in dry eye: a preliminary study. Eye 2005;19:1276-1279.
34. Benítez-Del-Castillo JM, Acosta MC, Wassf MA, et al. Relation between corneal innervation with confocal microscopy and corneal sensitivity with noncontact esthesiometry in patients with dry eye. Invest Ophthalmol Vis Sci. 2007 Jan;48:173-181.
35. De Paiva CS, Pfugfelder SC. Corneal epitheliopathy of dry eye induces hyperesthesia to mechanical air jet stimulation. Am J Ophthalmol. 2004;137:109-115.
36. Tuisku IS, Konttinen YT, Konttinen LM, Tervo TM. Alterations in corneal sensitivity and nerve morphology in patients with primary Sjögren's syndrome. Exp Eye Res. 2008;86:879-885.
37. Villani E, Galimberti D, Viola F, Mapelli C, Ratiglia R. The cornea in Sjogren's syndrome: an in vivo confocal study. Invest Ophthalmol Vis Sci. 2007 May;48:2017-2022.
38. Tuisku IS, Konttinen YT, Konttinen LM, Tervo TM. Corneal innervation and morphology in primary Sjögren's syndrome. Invest Ophthalmol Vis Sci. 2003;44:2545-2549.
39. Zhang M, Chen J, Luo L, Xiao Q, Sun M, Liu Z. Altered corneal nerves in aqueous tear defciency viewed by in vivo confocal microscopy. Cornea. 2005;24:818-824.
40. Benítez del Castillo JM, Wasfy MA, Fernandez C, Garcia-Sanchez J. An in vivo confocal masked study on corneal epithelium and subbasal nerves in patients with dry eye. Invest Ophthalmol Vis Sci. 2004;45:3030-3035.
41. Hamrah P, Cruzat A, Dastjerdi MH, Zheng L, Shahatit B, Bayhan HA, Dana R, Pavan-Langston D. Corneal Sensation and Subbasal Nerve Alterations in Patients with Herpes Simplex Keratitis: An In Vivo Confocal Microscopy Study. Ophthalmology. 2010; 117:1930-1936.
42. Dastjerdi MH, Hamrah P, Dana MR, Pavan-Langston D. Comparison of corneal nerve and corneal sensation in herpes zoster keratopathy with in vivo confocal microscopy. Invest Ophthalmol Vis Sci. 2007;48:3646. http://abstracts.iovs. org/cgi/content/abstract/48/5/3646, May 10, 2007.
43. Hamrah P, Cruzat A, Dastjerdi MH, Zheng L, Shahatit B, Bayhan HA, Dana R, Pavan-Langston D. Corneal sensation and subbasal nerve alterations in patients with Herpies Simplex Keratitis: An in vivo confocal microscopy study. Ophthalmology. 2010; 117:1930-1936.
44. Hamrah P, Schrems WA, Hoesl LM, Dastjerdi MH, Dana R, Pavan-Langston D. Corneal epithelial and stromal changes in patients with herpes simplex keratitis: An in vivo confocal microscopy study. Invest Ophthalmol Vis Sci. 2009;50:2389. http://abstracts.iovs.org/cgi/content/abstract/50/5/2389, April 11, 2008.
45. Kurbanyan K, Hoesl LM, Schrems WA, Hamrah P. Morphology and density of corneal nerves in acanthamoeba and fungal keratitis: An in vivo confocal microscopy study. Invest Ophthalmol Vis Sci. 2009;50:2402. http://abstracts. iovs. org/cgi/content/abstract/50/5/2402, April 11, 2009.
46. Cruzat A, Mantopoulos D, Zheng L, Hamrah P. In vivo confocal microscopy study of epithelial dendritic cells and subbasal nerve plexus in infectious keratitis. Boston, MA, 2009; 26th Biennial Cornea Conference Abstracts.
47. Patel DV, McGhee CN. In vivo laser scanning confocal microscopy confrms that the human corneal sub-basal nerve plexus is a highly dynamic structure. Invest Ophthalmol Vis Sci. 2008;49:3409-3412.
48. Richter A, Slowik C, Somodi S, Vick HP, Guthoff R. Corneal reinnervation following penetrating keratoplasty-cor-relation of esthesiometry and confocal microscopy. Ger J Ophthalmol. 1996 Nov;5:513-517.
49. Darwish T, Brahma A, Efron N, O'Donnell C. Subbasal nerve regeneration after penetrating keratoplasty. Cornea. 2007 Sep;26:935-940. (Pubitemid 47329796)
50. Niederer RL, Perumal D, Sherwin T, McGhee CN. Corneal innervation and cellular changes after corneal transplantation: an in vivo confocal microscopy study. Invest Ophthalmol Vis Sci. 2007;48:621-626.
51. Patel SV, Erie JC, McLaren JW, Bourne WM. Keratocyte density and recovery of subbasal nerves after penetrating keratoplasty and in late endothelial failure. Arch Ophthalmol. 2007;125:1693-1698.
52. Moilanen JA, Vesaluoma MH, Müller LJ, Tervo TM. Long-term corneal morphology after PRK by in vivo confocal microscopy. Invest Ophthalmol Vis Sci. 2003;44:1064-1069.
53. Erie JC, McLaren JW, Hodge DO, Bourne WM. Recovery of corneal subbasal nerve density after PRK and LASIK. Am J Ophthalmol. 2005;140:1059-1064.
54. Linna T, Tervo T. Real-time confocal microscopic observations on human corneal nerves and wound healing after excimer laser photorefractive keratectomy. Curr Eye Res. 1997;16:640-649.
55. Pérez-Santonja JJ, Sakla HF, Cardona C, Chipont E, Alió JL. Corneal sensitivity after photorefractive keratectomy and laser in situ keratomileusis for low myopia. Am J Ophthalmol. 1999;127:497-504.
56. Kauffmann T, Bodanowitz S, Hesse L, Kroll P. Corneal rein-nervation after photorefractive keratectomy and laser in situ keratomileusis: an in vivo study with a confocal videomi-croscope. Ger J Ophthalmol. 1996;5:508-512.
57. Perez-Gomez I, Efron N. Change to corneal morphology after refractive surgery (myopic laser in situ keratomileu-sis) as viewed with a confocal microscope. Optom Vis Sci. 2003;80:690-697.
58. Bragheeth MA, Dua HS. Corneal sensation after myopic and hyperopic LASIK: clinical and confocal microscopic study. Br J Ophthalmol. 2005;89:580-585.
59. Lee BH, McLaren JW, Erie JC, Hodge DO, Bourne WM. Reinnervation in the cornea after LASIK. Invest Ophthalmol Vis Sci. 2002;43:3660-3664.
60. Calvillo MP, McLaren JW, Hodge DO, Bourne WM. Corneal reinnervation after LASIK: prospective 3-year longitudinal study. Invest Ophthalmol Vis Sci. 2004;45:3991-3996.
61. Linna TU, Vesaluoma MH, Perez-Santonja JJ, Petroll WM, Alió JL, Tervo TM. Effect of myopic LASIK on corneal sensitivity and morphology of subbasal nerves. Invest Ophthalmol Vis Sci. 2000;41:393-397.
62. Sonigo B, Iordanidou V, Chong-Sit D, et al. In vivo corneal confocal microscopy comparison of intralase femtosecond laser and mechanical microkeratome for laser in situ ker-atomileusis. Invest Ophthalmol Vis Sci. 2006;47:2803-2811.
63. Darwish T, Brahma A, O'Donnell C, Efron N. Subbasal nerve fber regeneration after LASIK and LASEK assessed by non-contact esthesiometry and in vivo confocal microscopy: prospective study. J Cataract Refract Surg. 2007;33:1515-1521.
64. Darwish T, Brahma A, O'Donnell C, Efron N. Subbasal nerve fber regeneration after LASIK and LASEK assessed by noncontact esthesiometry and in vivo confocal microscopy: prospective study. J Cataract Refract Surg. 2007;33: 1515-1521.
65. Malik RA, Kallinikos P, Abbott CA, et al. Corneal confocal microscopy: a non-invasive surrogate of nerve fbre damage and repair in diabetic patients. Diabetologia 2003;46: 683-688.
66. Rosenberg ME, Tervo TM, Immonen IJ, Müller LJ, Grönhagen-Riska C, Vesaluoma MH. Corneal structure and sensitivity in type 1 diabetes mellitus. Invest Ophthalmol Vis Sci. 2000;41:2915-2921.
67. Kallinikos P, Berhanu M, O'Donnell C, Boulton AJ, Efron N, Malik RA. Corneal nerve tortuosity in diabetic patients with neuropathy. Invest Ophthalmol Vis Sci. 2004;45: 418-422.
68. Mehra S, Tavakoli M, Kallinikos PA, et al. Corneal confocal microscopy detects early nerve regeneration after pancreas transplantation in patients with type 1 diabetes. Diabetes Care. 2007;30:2608-2612.
69. Fraunfelder FW, Rich LF. Laser-assisted in situ ker-atomileusis complications in diabetes mellitus. Cornea. 2002;21:246-248.